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International Urogynecology Journal

https://doi.org/10.1007/s00192-019-03882-4

ORIGINAL ARTICLE

Birthweight and pelvic floor trauma after vaginal childbirth


Natalia Martinho 1 & Talia Friedman 2 & Friyan Turel 2 & Kirsty Robledo 3 & Cassio Riccetto 1 & Hans Peter Dietz 2,4

Received: 6 November 2018 / Accepted: 15 January 2019


# The International Urogynecological Association 2019

Abstract
Introduction and hypothesis Birthweight seems to be a risk factor for levator ani muscle (LAM) avulsion and a predictive factor
for pelvic organ prolapse (POP). Most trauma seems due to first vaginal birth.
Methods One thousand one hundred twenty-five women with at least two vaginal deliveries underwent a physician-directed
interview, followed by clinical examination (digital palpation and Pelvic Organ Prolapse Quantification-POPQ) and 4D
translabial ultrasound. Ultrasound volume data were obtained at rest, on pelvic floor contraction and Valsalva. The investigator,
blinded to all other data, performed offline analysis of the LAM integrity and hiatal area on Valsalva. We tested for associations
between birthweight of the first and of the largest vaginally born baby on the one hand and avulsion and symptoms/signs of
prolapse on the other hand.
Results Between July 2014 and July 2017, 1575 patients were seen. After exclusion of nulliparae and women with just one
vaginal birth, 1202 remained. Another 77 were excluded due to missing data, leaving 1125. A significant association was found
between birthweight and LAM avulsion as well as significant prolapse on POPQ. The birthweight of the first vaginally born baby
was at least as predictive for avulsion as the birthweight of any subsequent births, even when adjusted for maternal age at first
delivery and use of forceps.
Conclusions The birthweight of the first vaginally born baby is associated with levator avulsion and subsequent POP. Maximum
weight of vaginal births does not seem to be a stronger predictor.

Keywords Birthtrauma . Birthweight . Levator ani muscle avulsion . Pelvic floor . Pelvic organ prolapse . Ultrasound

Introduction exerted by the passage of the fetal head, which is enhanced


by maternal pushing [5, 6]. Such stretch, which is clearly more
Vaginal childbirth is the primary environmental factor in the than what can be tolerated by normal skeletal muscle [5], may
etiology of female pelvic organ prolapse (POP), at least partly lead to injuries of the levator ani muscle in some women,
mediated by trauma to the levator ani muscle [1–4]. During ranging from irreversible hyperdistension of the levator hiatus
the second stage of labor, the pelvic floor muscles undergo a (microtrauma) to avulsion (macrotrauma) [7, 8].
remarkable degree of soft tissue stretch due to the pressure Levator ani muscle avulsion is characterized by a complete
traumatic detachment of the puborectalis muscle from its in-
Presentation at a conference/meeting This work was presented at the sertion to the inferior pubic ramus [7, 8]. This trauma is asso-
IUGA 43rd Annual Meeting, Vienna, Austria, from June 27 to 30, 2018. ciated with pelvic organ prolapse [1–4] and its recurrence after
reconstructive surgery [9].
* Hans Peter Dietz Major risk factors of levator trauma are first vaginal deliv-
hpdietz@bigpond.com ery [10, 11], advanced maternal age at first delivery (>
35 years) [12] and use of forceps [13]. It is suggested that
1
Faculty of Medical Sciences, State University of Campinas –
UNICAMP, Campinas, Brazil birthweight may also be a risk factor for levator trauma [14]
2 and a predictor for prolapse stage and symptoms [15]. It is
Sydney Medical School Nepean, University of Sydney,
Sydney, Australia however not clear whether it is the weight of the firstborn or
3 the weight of the heaviest baby that is more important for the
NHMRC Clinical Trials Centre, University of Sydney,
Sydney, Australia etiology of levator trauma. Thus, we tested for associations
4 between birthweight of the first and of the largest vaginally
Sydney Medical School Nepean, Nepean Hospital,
Penrith, NSW 2750, Australia born baby on the one hand and avulsion and symptoms/signs
Int Urogynecol J

of prolapse on the other. Our study aimed to test the hypoth- Ultrasound data analysis
esis: ‘The birthweight of the heaviest vaginally born baby has
a stronger association with LAM avulsion than the Offline analysis of ultrasound volume data sets was performed
birthweight of the first vaginal birth.’ using the 4D View 10.0 software (GE Medical Ultrasound,
Ryde NSW, Australia) by the first author, blinded to all other
data, 3 months to 3 years after the imaging volume data had
Materials and methods been obtained and stored. A test-retest series performed prior
to commencing measurements for the study yielded a coeffi-
Design, setting and participants cient of Kappa’s agreement of 0.875 between the first and last
author, showing good agreement for the diagnosis of avulsion.
This was a retrospective study involving ultrasound data sets Levator ani muscle integrity was evaluated using tomo-
of 1125 vaginally parous women seen routinely at two tertiary graphic ultrasound imaging (TUI) of volumes obtained on
urogynecological centers between July 2014 and July 2017. maximum PFM contraction. Eight slices were obtained in
Our inclusion criteria were women who had had at least two the axial plane at 2.5-mm slice intervals, from 5 mm below
vaginal childbirths. Women who had no information regard- to 12.5 mm above the plane of minimal hiatal dimensions
ing their babies’ birthweight were excluded. This study was [20]. A complete levator avulsion was diagnosed if at least
approved by the local Human Research Ethics Committee the three central slices (i.e. the plane of minimal dimension
(NBMLHD HREC 13–70). plus slices 2.5 mm and 5 mm cranial to this plane—slices 3 to
5) showed an abnormal muscle insertion on the inferior pubic
ramus [21], as shown in Fig. 1.
Outcome measures Hiatal area was measured at the plane of minimal hiatal
dimensions, defined in the midsagittal plane as the minimal
Personal, clinical and obstetric data distance between the symphysis pubis and the anterior margin
of the central aspect of the puborectalis muscle [22].
All women underwent a standardized clinical assessment
which included a physician-directed interview and patient- Statistical analysis
reported personal, clinical and obstetric data. The following
characteristics were investigated: age, body mass index, pari- Statistical analysis was performed by the NHMRC Clinical
ty, delivery mode, birthweight, previous surgical history and Trials Centre of the University of Sydney using the program
presence of urinary and POP symptoms. The average time SPSS (Statistical Package for the Social Sciences) and
span between the birth of the first child and the assessment adopting a significance level of 5% (p < 0.05). We tested for
was 33.4 (range, 0.7–69.7) years. We did not obtain informa- association between birthweight of the first vaginally born
tion on the timing of subsequent births. All reported personal, baby and maximum birthweight of any vaginally born baby
clinical and obstetric data were obtained on the same day. with symptoms and signs of POP and levator avulsion, using
two sample t-tests and Pearson’s correlation. Univariate and
Pelvic floor assessment multivariate logistic regressions were used to quantify the
contribution of each of these birthweight variables on levator
Digital palpation was performed to assess PFM contractility, avulsion. Multivariate analyses were adjusted for maternal age
which was graded according to the Modified Oxford Grading at first delivery and use of forceps, with each model’s perfor-
scale (range 0 to 5) [16]. POP was quantified for each com- mance estimated with the area under the receiver-operator
partment separately (anterior, middle, posterior) using the characteristic (ROC) curve. The difference between two areas
Pelvic Organ Prolapse Quantification (POPQ) system (range under the ROC curves was analyzed as described by DeLong
from stage 0 to 4) [17]. POPQ stage 2 or higher for anterior and collaborators (1988) [23] to test the hypothesis: ‘The
and posterior vaginal wall as well as POPQ stage I or higher maximum weight of any vaginally born baby is a stronger
for the uterus were considered clinically relevant and classi- predictor for avulsion compared to the birthweight of the first
fied as a significant prolapse on POPQ [18]. vaginal birth.’
Following this, 4D translabial ultrasound (TLUS) was per-
formed with women in the supine position, after voiding,
using a GE Voluson 730 Expert system (GE Medical, Kretz, Results
Austria) with an 8–4 MHz curved array volume transducer.
Volume acquisition was performed with an acquisition angle Between July 2014 and July 2017, 1575 consecutive patients
of 85 degrees, at rest, on pelvic floor muscle (PFM) contrac- were seen at two tertiary urogynecological centers. Of those,
tion and maximum Valsalva [19]. 23 had missing ultrasound volumes, 373 were nulliparous or
Int Urogynecol J

Fig. 1 Right-sided complete


avulsion, indicated by an asterisk
(*). A complete levator avulsion
is diagnosed if at least the three
central slices (slices 3 to 5) show
an abnormal muscle insertion on
the inferior pubic ramus

had just one vaginal delivery, and 54 did not have data regard- During Valsalva, the mean hiatal area was 29.8 cm2 (SD
ing their babies’ birthweights and were excluded from the 9.7). Complete levator avulsion was found in 293 women
study. Therefore, the final sample was composed of 1125 par- (26%), and it was bilateral in 134 (11.9%). Table 2 shows
ous women, and all reported data pertain to this population the association between the birthweight of the first vaginally
unless otherwise indicated. born baby and the maximum weight of any vaginally born
Mean age was 57.1 ± 12.5 years old (range 24.2 to 89.7), baby with levator avulsion and symptoms and signs of pro-
and mean body mass index was 29.5 ± 6.3 kg/m2 (range 15.7 lapse. There was no significant difference in birthweight re-
to 58.8). All patients were parous women who had had at least garding the type of avulsion (uni- or bilateral) on subgroup
two vaginal births and 371 (33%) at least one forceps delivery. analysis.
The mean birthweight of the first vaginally born baby was Subsequent births were heavier than the first in 456/1125
3362 g (range, 459–5000 g); the average weight of the heavi- (40.5%). These women did not have a higher risk of avulsion
est vaginally born child was 3775 g (range, 1786–5900 g). than those with smaller subsequent births. The odds for leva-
Three hundred ninety-four (35%) had had a hysterectomy tor ani muscle avulsion are 1.36 times greater for those women
since their last birth, 144 (12.8%) incontinence surgery and in whom the first baby was the heaviest compared with those
236 (21%) prolapse surgery. Eight hundred eighteen (72.7%) who had a heavier baby in a subsequent delivery, even when
reported symptoms of stress incontinence, 842 (74.8%) of adjusted for maternal age at first delivery and use of forceps
urge incontinence, 289 (25.7%) of increased urinary frequen- (p = 0.03) (Table 3).
cy, 433 (38.5%) of nocturia and 374 (33.2%) of voiding The birthweight of the first vaginally born baby is a
dysfunction. better univariate predictor for levator avulsion (AUC =
Clinical examination was possible in 1124 women. On 0.574) compared with the maximum weight of any vagi-
POPQ examination (Table 1), 693 (61.6%) had a significant nally born baby (AUC = 0.540). We created two models for
cystocele, 220 (37.5%) significant uterine prolapse and 646 the prediction of avulsion, containing known predictors
(52.8%) significant descent of the posterior vaginal wall. The such as forceps and age at first birth, and then added either
Gh + Pb measure was abnormal (≥ 7 cm) [24] in 905 women the birthweight of the firstborn or the birthweight of the
(80%). The Modified Oxford Scale was used to grade the heaviest baby. When adjusted for maternal age at first de-
pelvic floor muscle contractility, resulting in a mean grading livery and use of forceps, the area under the curve (AUC)
of 2.1 (range 0–5) on the right and 2.3 (range 0–5) on the left. for the birthweight of the first vaginally born baby was
On digital palpation, a unilateral avulsion was found in 170 0.634 (model 1) and the AUC for the maximum weight
women (15.1%) while bilateral avulsion was found in 128 of any vaginally born baby was 0.628 (model 2). This
women (11.4%). difference was not significant (p = 0.473). Hence, we were
Int Urogynecol J

Table 1 Clinical examination of pelvic organs descent associated with a significant increase in the odds of levator
Mean ± SD (range) avulsion [10].
(in centimeters) The baby’s birthweight is strongly associated with head
circumference (r = 0,749; p < 0.001) [26] and therefore is
Pelvic Organ Prolapse Ba −0.6 ± 1.6 (−3 to 7.5) closely linked to the degree of stretching of the puborectalis
Quantification-POPQ n = 1124 C −4.2 ± 2.9 (−11 to 8) muscle during vaginal delivery [27]. It is not surprising there-
Bp −0.9 ± 1.3 (−3 to 8) fore that larger head circumference seems to be associated
Gh 4.5 ± 1.2 (1.5 to 10) with increased length of the second stage of labor [26].
Pb 3.4 ± 0.8 (1 to 7) In this study, if the first vaginally born baby was also the
heaviest one, this was found to be a significant risk factor for
Data are presented as mean and standard deviation (SD)
levator avulsion with an odds ratio of 1.36 (p = 0.03). Even
when adjusted for maternal age at first delivery and use of
not able to prove our hypothesis (‘the birthweight of any
forceps, the association between first birthweight and avulsion
vaginally born baby is a stronger predictor for avulsion
remained significant (AUC = 0.634) although not significant-
compared to the birthweight of the first vaginal birth’).
ly stronger than the maximum weight of any vaginally born
baby (AUC = 0.628).
It is plausible that tissues that are unable to stretch with a
Discussion given distension because of the individual biomechanical prop-
erties of the mother will rupture at the time of a first birth.
This study has demonstrated a significant relationship be- Biomechanical properties clearly vary enormously. [27]. The
tween birthweight and major levator trauma (levator avulsion) second birth will be easier because the rupture has already
as well as significant prolapse on POPQ in women presenting occurred with the first, and further trauma may then be unlikely.
for treatment of pelvic floor dysfunction over 30 years after a On the other hand, if tissues survived intact the first time, they
first vaginal birth. The birthweight of the first vaginally born probably will not rupture at the time of a second birth. This is
baby was at least as predictive for levator avulsion as the consistent with evidence from observational studies [10, 11].
maximum weight of any subsequent vaginally born baby, re- Current literature is contradictory regarding the association
futing our hypothesis. between birthweight and obstetric trauma and the predisposi-
The first vaginal delivery seems to be the crucial moment tion to POP occurrence [28, 29]. Delivery of infants over
for levator trauma [10, 11], which occurs in approximately 4000 g seems associated with Obstetric Anal Sphincter
10–35% of women giving birth vaginally in the developed Injury (OASIS) [30] and pelvic floor dysfunction [31].
world [8], although trauma rates may be substantially lower Valsky and collaborators (2009) [26] showed that, for
in populations with traditional reproductive behavior [25]. birthweight > 3400 g, the odds of levator avulsion increased
Additional pregnancies and vaginal births do not seem to be by a factor of 1.094 (p = 0.028) for every 100 g increase.

Table 2 Association between birthweight and levator avulsion and signs and symptoms of prolapse

Birthweight of the first Maximum weight of any


vaginally born baby (g) vaginally born baby (g)

Symptoms of prolapse (mean ± SD)1 Yes (n = 619) 3377 (± 0.563) vs 3343 (± 0.578) p = 0.33 3693 (± 0.557) vs 3696 (± 0.562) p = 0.91
No (n = 506)
Significant prolapse on POPQ (M ± SD)1 Yes (n = 919) 3377 (± 0.568) vs 3292 (± 0.573) p = 0.05 3711 (± 0.571) vs 3618 (± 0.495) p = 0.03
No (n = 205)
Levator ani muscle avulsion1§ Yes (n = 293) 3467 (± 0.553) vs 3324 (± 0.571) p < 0.001 3755 (± 0.536) vs 3673 (± 0.565) p = 0.03
No (n = 832)
Hiatal area on Valsalva (n = 1124)2 p < 0.001; r = 0.13 p < 0.001; r = 0.15

Data are presented as mean and standard deviation (SD)


§
Considering complete unilateral (right or left) or bilateral avulsion
POPQ = Pelvic Organ Prolapse Quantification
1
t-test was used. 2 Pearson’s correlation test was used
Int Urogynecol J

Table 3 Birthweight and risk of levator ani muscle avulsion References


First baby Any other p OR 95% CI
heaviest subsequent value1 1. Dietz HP, Franco AV, Shek KL, Kirby A. Avulsion injury and
n = 669 birth heaviest levator hiatal ballooning: two independent risk factors for prolapse?
n = 456 An observational study. Acta Obstet Gynecol Scand. 2012;91(2):
211–4. https://doi.org/10.1111/j.1600-0412.2011.01315.x.
Avulsion No 511 (76.4%) 321 (70.4%) 0.03 1.36 1.04–1.78 2. Van Delft K, Sultan AH, Thakar R, Schwertner-Tiepelmann N,
Yes 158 (23.6%) 135 (29.6%) Kluivers K. The relationship between postpartum levator ani mus-
cle avulsion and signs and symptoms of pelvic floor disorders.
1
Chi-square test; OR: odds ratio; 95% CI: 95% confidence interval. n = 1125 BJOG. 2014;121(9):1164–71. https://doi.org/10.1111/1471-0528.
12666.
3. Volløyhaug I, Mørkved S, Salvessen KA. Association between pel-
vic floor muscle trauma and pelvic organ prolapse 20 years after
Several limitations of our study need to be mentioned. delivery. Int Urogynecol J. 2016;27(1):39–45. https://doi.org/10.
Obstetric data, including birthweight, were patient-reported, 1007/s00192-015-2784-8.
and this may have led to recall bias. This is particularly true 4. Abdool Z, Dietz HP, Lindeque BG. Prolapse symptoms are associ-
in view of the fact that the average time span between the birth ated with abnormal functional anatomy of the pelvic floor. Int
Urogynecol J. 2017;28(9):1387–91. https://doi.org/10.1007/
of the first child and the assessment was 33.4 (range, 0.7– s00192-017-3280-0.
69.7) years. 5. Lien KC, Mooney B, DeLancey JO, Ashton-Miller JA. Levator ani
In addition, we did not have information on some char- muscle stretch induced by simulated vaginal birth. Obstet Gynecol.
acteristics of labor that may also influence the likelihood 2004;103(1):31–40. https://doi.org/10.1097/01.AOG.0000109207.
22354.65.
of levator ani trauma and act as confounders, such as
6. Svabik K, Shek KL, Dietz HP. How much does the puborectalis
length of the second stage of labor, fetal head circumfer- muscle have to stretch during childbirth? BJOG. 2009;116(12):
ence, malposition or the occurrence of obstructed labor. 1657–62. https://doi.org/10.1111/j.1471-0528.2009.02321.x.
Moreover, due to the above-mentioned long latency of 7. Shek KL, Dietz HP. The effect of childbirth on hiatal dimensions.
33.4 years, our findings clearly represent past rather than Obstet Gynecol. 2009;113(6):1272–8. https://doi.org/10.1097/
AOG.0b013e3181a5ef23.
present obstetric practice, which may also have influenced 8. Dietz HP. Pelvic floor trauma in childbirth. Aust N Z J Obstet
results. Due to this long latency, other factors such as Gynaecol. 2013;53(3):220–30. https://doi.org/10.1111/ajo.12059.
chronic constipation, smoking, asthma and menopause 9. Friedman T, Eslick G, Dietz HP. Risk factors for prolapse
may have influenced our findings. However, menopausal recurrence—systematic review and meta-analysis. Int Urogynecol
J. 2018;29(1):13–21. https://doi.org/10.1007/s00192-017-3475-4.
status seems unlikely to impact pelvic floor functional
10. Horak TA, Guzman-Rojas R, Shek KL, Dietz HP. Pelvic floor trau-
biometry [32], and the same seems true for asthma and ma: does the second baby matter? Ultrasound Obstet Gynecol.
smoking (unpublished own data). 2014;44(1):90–4. https://doi.org/10.1002/uog.13252.
Finally, it needs to be mentioned that the majority of our 11. Kamisan Atan I, Lin S, Herbison P, Dietz HP. Wilson PD for the
patients were Caucasian and symptomatic of pelvic floor dys- PROLONG study group: it is the first birth that does the damage: a
cross-sectional study 20 years after delivery. Int Urogynecol J.
function, limiting the validity of our findings for other 2018;29:1637–43. https://doi.org/10.1007/s00192-018-3616-4.
populations. 12. Rahmanou P, Caudwell-Hall J, Kamisan Atan I, Dietz HP. The
In conclusion, birthweight is significantly associated with association between maternal age at first delivery and risk of ob-
levator avulsion and subsequent pelvic organ prolapse, espe- stetric trauma. Am J Obstet Gynecol. 2016;215(4):451.e1–7.
https://doi.org/10.1016/j.ajog.2016.04.032.
cially the birthweight of the first vaginally born baby.
13. Dietz HP. Forceps: towards obsolescence or revival? Acta Obstet
Maximum birthweight is also predictive, but clearly not more Gynecol Scand. 2015;94(4):347–51. https://doi.org/10.1111/aogs.
so than the weight of the first vaginally born child. 12592.
14. Garcia-Mejido JA, Gutierrez-Palomino L, Borrero C, Valdivieso P,
Funding The first author was the recipient of a scholarship sponsored by Fernandez-Palacin A, Sainz-Bueno JA. Factors that influence the
the Foundation of Research Support of the State of Sao Paulo, Brazil development of avulsion of the levator ani muscle in eutocic deliv-
(FAPESP process 2015/22521–8 and 2017/02565–6) during her visit at eries: 3-4D transperineal ultrasound study. J Matern Fetal Neonatal
the Pelvic Floor Unit, Nepean Hospital, University of Sydney, Australia. Med. 2016;29(19):3183–6. https://doi.org/10.3109/14767058.
2015.1118041.
15. Rodriguez-Mias NL, Martinez-Franco E, Aguado J, Sanchez E,
Compliance with ethical standards Amat-Tardiu L. Pelvic organ prolapse and stress urinary inconti-
nence: do they share the same risk factors? Eur J Obstet Gynecol
Conflicts of interest HP Dietz has received paid travel expenses and Reprod Biol. 2015;190:52–7. https://doi.org/10.1016/j.ejogrb.
honoraria from GE Medical. 2015.04.015.
16. Laycock J, Jerwood D. Pelvic floor muscle assessment: the
Publisher’s note Springer Nature remains neutral with regard to jurisdic- PERFECT scheme. Physiotherapy. 2001;87(12):631–42. https://
tional claims in published maps and institutional affiliations. doi.org/10.1016/S0031-9406(05)61108-X.
Int Urogynecol J

17. Bump RC, Mattiasson A, Bø K, et al. The standardization of termi- 26. Valsky DV, Lipschuetz M, Bord A, et al. Fetal head circumference
nology of female pelvic organ prolapse and pelvic floor dysfunc- and length of second stage of labor are risk factors for levator ani
tion. Am J Obstet Gynecol. 1996;175(1):10–7. muscle injury, diagnosed by 3-dimensional transperineal ultrasound
18. Dietz HP. Pelvic organ prolapse—a review. Aust Fam Physician. in primiparous women. Am J Obstet Gynecol. 2009;201(1):91.e1–
2015;44(7):446–52. 7. https://doi.org/10.1016/j.ajog.2009.03.028.
19. Dietz HP. Pelvic floor ultrasound: a review. Clin Obstet Gynecol. 27. Svabik K, Shek KL, Dietz HP. How much does the puborectalis
2017;60(1):58–81. https://doi.org/10.1097/GRF.0000000000000264. muscle have to stretch during childbirth? BJOG. 2009;116:1657–62.
20. Dietz HP, Shek KL. Tomographic ultrasound imaging of the pelvic 28. Tegerstedt G, Miedel A, Mæhle-Schmidt M, Nyrén O,
floor: which levels matter most? Ultrasound Obstet Gynecol. Hammarstrom M. Obstetric risk factors for symptomatic prolapse:
2009;33(6):698–703. https://doi.org/10.1002/uog.6403. a population-based approach. Am J Obstet Gynecol. 2006;194(1):
21. Dietz HP, Bernardo MJ, Kirby A, Shek KL. Minimal criteria for the 75–81. https://doi.org/10.1016/j.ajog.2005.06.086.
diagnosis of avulsion of the puborectalis muscle by tomographic 29. Swift SE, Pound T, Dias JK. Case-control study of etiologic factors
ultrasound. Int Urogynecol J. 2011;22(6):699–704. https://doi.org/ in the development of severe pelvic organ prolapse. Int Urogynecol
10.1007/s00192-010-1329-4. J Pelvic Floor Dysfunct. 2001;12(3):187–92.
22. Dietz HP, Wong V, Shek KL. A simplified method for determining 30. Kapaya H, Hashim S, Jha S. OASI: a preventable injury? Eur J
hiatal biometry. Aust N Z J Obstet Gynaecol. 2011;51(6):540–3. Obstet Gynecol Reprod Biol. 2015;185:9–12. https://doi.org/10.
https://doi.org/10.1111/j.1479-828X.2011.01352.x. 1016/j.ejogrb.2014.11.023.
23. DeLong ER, DeLong DM, Clarke-Pearson DL. Comparing the
31. Wilson D, Dornan J, Milsom I, Freeman R. UR-CHOICE: can we
areas under two or more correlated receiver operating characteristic
provide mothers-to-be with information about the risk of future
curves: a nonparametric approach. Biometrics. 1988;44(3):837–45.
pelvic floor dysfunction? Int Urogynecol J. 2014;25(11):1449–52.
24. Girgis B, Kamisan Atan I, Shek KL, Dietz HP. How to determine
https://doi.org/10.1007/s00192-014-2376-z.
“ballooning” of the levator hiatus on clinical examination: a retro-
spective observational study. Int Urogynecol J. 2013;24(11):1933– 32. Trutnowski G, Guzman Rojas R, Martin A, Dietz HP. Pelvic floor
7. https://doi.org/10.1007/s00192-013-2119-6. dysfunction—the role of menopause. Maturitas. 2013 Oct;76(2):
25. Turel F, Caagbay D, Dietz HP. The prevalence of major birth trauma 134–8.
in Nepali women. J Ultrasound Med. 2018; Accepted 27.2.18.

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